#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Acetyltransferase Enok regulates transposon silencing and piRNA cluster transcription


Autoři: Shih-Ying Tsai aff001;  Fu Huang aff001
Působiště autorů: Institute of Biological Chemistry, Academia Sinica, Taipei, Taiwan aff001
Vyšlo v časopise: Acetyltransferase Enok regulates transposon silencing and piRNA cluster transcription. PLoS Genet 17(2): e1009349. doi:10.1371/journal.pgen.1009349
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009349

Souhrn

The piRNA pathway is a highly conserved mechanism to repress transposon activation in the germline in Drosophila and mammals. This pathway starts from transcribing piRNA clusters to generate long piRNA precursors. The majority of piRNA clusters lack conventional promoters, and utilize heterochromatin- and HP1D/Rhino-dependent noncanonical mechanisms for transcription. However, information regarding the transcriptional regulation of piRNA clusters is limited. Here, we report that the Drosophila acetyltransferase Enok, which can activate transcription by acetylating H3K23, is critical for piRNA production from 54% of piRNA clusters including 42AB, the major piRNA source. Surprisingly, we found that Enok not only promotes rhino expression by acetylating H3K23, but also directly enhances transcription of piRNA clusters by facilitating Rhino recruitment. Taken together, our study provides novel insights into the regulation of noncanonical transcription at piRNA clusters and transposon silencing.

Klíčová slova:

Cloning – DAPI staining – Eggs – Gene expression – Genomics – Ovaries – Transcriptional control – Transposable elements


Zdroje

1. Fedoroff NV. Presidential address. Transposable elements, epigenetics, and genome evolution. Science. 2012; 338(6108):758–67. doi: 10.1126/science.338.6108.758 23145453.

2. Holoch D, Moazed D. RNA-mediated epigenetic regulation of gene expression. Nature reviews Genetics. 2015;16(2):71–84. doi: 10.1038/nrg3863 25554358; PubMed Central PMCID: PMC4376354.

3. Fejes Tóth K, Pezic D, Stuwe E, Webster A. The piRNA Pathway Guards the Germline Genome Against Transposable Elements. Advances in experimental medicine and biology. 2016;886:51–77. doi: 10.1007/978-94-017-7417-8_4 26659487; PubMed Central PMCID: PMC4991928.

4. Fu Q, Wang PJ. Mammalian piRNAs: Biogenesis, function, and mysteries. Spermatogenesis. 2014;4:e27889. doi: 10.4161/spmg.27889 25077039; PubMed Central PMCID: PMC4114582.

5. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–103. Epub 2007/03/10. S0092-8674(07)00257-7[pii] doi: 10.1016/j.cell.2007.01.043 17346786.

6. Andersen PR, Tirian L, Vunjak M, Brennecke J. A heterochromatin-dependent transcription machinery drives piRNA expression. Nature. 2017;549(7670):54–9. doi: 10.1038/nature23482 28847004; PubMed Central PMCID: PMC5590728.

7. Zanni V, Eymery A, Coiffet M, Zytnicki M, Luyten I, Quesneville H, et al. Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters. Proc Natl Acad Sci U S A. 2013;110(49):19842–7. doi: 10.1073/pnas.1313677110 24248389; PubMed Central PMCID: PMC3856796.

8. Huang X, Fejes Toth K, Aravin AA. piRNA Biogenesis in Drosophila melanogaster. Trends in genetics: TIG. 2017;33(11):882–94. doi: 10.1016/j.tig.2017.09.002 28964526.

9. Czech B, Hannon GJ. One Loop to Rule Them All: The Ping-Pong Cycle and piRNA-Guided Silencing. Trends in biochemical sciences. 2016;41(4):324–37. doi: 10.1016/j.tibs.2015.12.008 26810602; PubMed Central PMCID: PMC4819955.

10. Rozhkov NV, Hammell M, Hannon GJ. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev. 2013;27(4):400–12. doi: 10.1101/gad.209767.112 23392609; PubMed Central PMCID: PMC3589557.

11. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 2013;27(4):390–9. doi: 10.1101/gad.209841.112 23392610; PubMed Central PMCID: PMC3589556.

12. Akkouche A, Mugat B, Barckmann B, Varela-Chavez C, Li B, Raffel R, et al. Piwi Is Required during Drosophila Embryogenesis to License Dual-Strand piRNA Clusters for Transposon Repression in Adult Ovaries. Mol Cell. 2017;66(3):411–9 e4. doi: 10.1016/j.molcel.2017.03.017 28457744.

13. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, et al. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 2006;20(16):2214–22. doi: 10.1101/gad.1454806 16882972; PubMed Central PMCID: PMC1553205.

14. Mohn F, Sienski G, Handler D, Brennecke J. The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell. 2014;157(6):1364–79. doi: 10.1016/j.cell.2014.04.031 24906153.

15. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell. 2009;138(6):1137–49. doi: 10.1016/j.cell.2009.07.014 19732946; PubMed Central PMCID: PMC2770713.

16. Zhang Z, Wang J, Schultz N, Zhang F, Parhad SS, Tu S, et al. The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell. 2014;157(6):1353–63. doi: 10.1016/j.cell.2014.04.030 24906152; PubMed Central PMCID: PMC4167631.

17. Hur JK, Luo Y, Moon S, Ninova M, Marinov GK, Chung YD, et al. Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in Drosophila. Genes Dev. 2016;30(7):840–55. doi: 10.1101/gad.276030.115 27036967; PubMed Central PMCID: PMC4826399.

18. Chen YA, Stuwe E, Luo Y, Ninova M, Le Thomas A, Rozhavskaya E, et al. Cutoff Suppresses RNA Polymerase II Termination to Ensure Expression of piRNA Precursors. Mol Cell. 2016;63(1):97–109. doi: 10.1016/j.molcel.2016.05.010 27292797; PubMed Central PMCID: PMC4980073.

19. Huang F, Abmayr SM, Workman JL. Regulation of KAT6 acetyltransferases and their roles in cell cycle progression, stem cell maintenance, and human disease. Mol Cell Biol. 2016. doi: 10.1128/MCB.00055-16 27185879.

20. Huang F, Paulson A, Dutta A, Venkatesh S, Smolle M, Abmayr SM, et al. Histone acetyltransferase Enok regulates oocyte polarization by promoting expression of the actin nucleation factor spire. Genes Dev. 2014;28(24):2750–63. Epub 2014/12/17. doi: 10.1101/gad.249730.114 [pii]. 25512562; PubMed Central PMCID: PMC4265678.

21. Feller C, Forne I, Imhof A, Becker PB. Global and specific responses of the histone acetylome to systematic perturbation. Mol Cell. 2015;57(3):559–71. doi: 10.1016/j.molcel.2014.12.008 25578876.

22. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003;17(15):1870–81. Epub 2003/08/05. doi: 10.1101/gad.1110503 [pii]. 12897054; PubMed Central PMCID: PMC196235.

23. Xin T, Xuan T, Tan J, Li M, Zhao G. The Drosophila putative histone acetyltransferase Enok maintains female germline stem cells through regulating Bruno and the niche. Dev Biol. 2013;384(1):1–12. Epub 2013/10/15. doi: 10.1016/j.ydbio.2013.10.001 S0012-1606(13)00532-0 [pii]. 24120347

24. Chou TB, Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics. 1996;144(4):1673–9. Epub 1996/12/01. 8978054; PubMed Central PMCID: PMC1207718.

25. Czech B, Preall JB, McGinn J, Hannon GJ. A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell. 2013;50(5):749–61. Epub 2013/05/15. doi: 10.1016/j.molcel.2013.04.007 S1097-2765(13)00288-8 [pii]. 23665227; PubMed Central PMCID: PMC3724427.

26. Sienski G, Donertas D, Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 2012;151(5):964–80. Epub 2012/11/20. doi: 10.1016/j.cell.2012.10.040 [pii]. 23159368; PubMed Central PMCID: PMC3504300.

27. Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell. 2013;50(5):736–48. doi: 10.1016/j.molcel.2013.04.006 23665228; PubMed Central PMCID: PMC3724422.

28. Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, et al. The genetic makeup of the Drosophila piRNA pathway. Mol Cell. 2013;50(5):762–77. doi: 10.1016/j.molcel.2013.04.031 23665231; PubMed Central PMCID: PMC3679447.

29. Han BW, Wang W, Zamore PD, Weng Z. piPipes: a set of pipelines for piRNA and transposon analysis via small RNA-seq, RNA-seq, degradome- and CAGE-seq, ChIP-seq and genomic DNA sequencing. Bioinformatics. 2015;31(4):593–5. doi: 10.1093/bioinformatics/btu647 25342065; PubMed Central PMCID: PMC4325541.

30. Jin Y, Tam OH, Paniagua E, Hammell M. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics. 2015;31(22):3593–9. doi: 10.1093/bioinformatics/btv422 26206304; PubMed Central PMCID: PMC4757950.

31. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308; PubMed Central PMCID: PMC2796818.

32. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281; PubMed Central PMCID: PMC4302049.

33. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 22388286; PubMed Central PMCID: PMC3322381.

34. Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44(W1):W160–5. doi: 10.1093/nar/gkw257 27079975; PubMed Central PMCID: PMC4987876.

35. Sato K, Nishida KM, Shibuya A, Siomi MC, Siomi H. Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev. 2011;25(22):2361–73. Epub 2011/11/17. doi: 10.1101/gad.174110.111 [pii]. 22085963; PubMed Central PMCID: PMC3222902.

36. Zhang Z, Xu J, Koppetsch BS, Wang J, Tipping C, Ma SM, et al. Heterotypic piRNA Ping-Pong Requires Qin, a Protein with Both E3 Ligase and Tudor Domains (vol 44, pg 572, 2011). Molecular Cell. 2011;44(6):1005–. doi: 10.1016/j.molcel.2011.12.002 WOS:000298827200019.

37. Wang SH, Elgin SC. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci U S A. 2011;108(52):21164–9. doi: 10.1073/pnas.1107892109 22160707; PubMed Central PMCID: PMC3248523.


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 3/2024 (znalostní test z časopisu)
nový kurz

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Aktuální možnosti diagnostiky a léčby litiáz
Autoři: MUDr. Tomáš Ürge, PhD.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#